Fluid shear stress-induced osteoarthritis: Roles of cyclooxygenase-2 and its metabolic products in inducing the expression of proinflammatory cytokines and matrix metalloproteinases

FASEB Journal

Volumn 27, Issue 12, 2013, Pages 4664-4677

  Wang, Pu ^a,b   Guan, Pei Pei ^a,b   Guo, Chuang ^a   Zhu, Fei ^b   Konstantopoulos, Konstantinos ^b,c,d   Wang, Zhan You ^a  

^a NORTHEASTERN UNIVERSITY   (China)

^b Department of Chemical and Biomolecular Engineering ^*  (United States)

^c Johns Hopkins Physical Sciences Oncology Center   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

15d PGJ2; Apoptosis; Chondrocytes; Inflammation; PGE2

Indexed keywords

CYCLOOXYGENASE 2; CYTOKINE; MATRIX METALLOPROTEINASE; PROSTAGLANDIN E2;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; CARTILAGE CELL; DISEASE COURSE; DISEASE SEVERITY; DOWN REGULATION; GENE MUTATION; HUMAN; NONHUMAN; OSTEOARTHRITIS; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SHEAR STRESS; UPREGULATION;

15D-PGJ2; APOPTOSIS; CHONDROCYTES; INFLAMMATION; PGE2;

ANIMALS; CYCLOOXYGENASE 2; CYTOKINES; HUMANS; MATRIX METALLOPROTEINASES; OSTEOARTHRITIS; STRESS, MECHANICAL;

EID: 84890482110     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-234542     Document Type: Review

References (100)

1. Carter, D. R., Beaupre, G. S., Wong, M., Smith, R. L., Andriacchi, T. P., and Schurman, D. J. (2004) The mechanobiology of articular cartilage development and degeneration. Clin. Orthop. Relat. Res., S69-S77
2. Buckwalter, J. A., Martin, J. A., and Brown, T. D. (2006) Perspectives on chondrocyte mechanobiology and osteoarthritis. Biorheology 43, 603-609
3. Yokota, H., Goldring, M. B., and Sun, H. B. (2003) CITED2-mediated regulation of MMP-1 and MMP-13 in human chondrocytes under flow shear. J. Biol. Chem. 278, 47275-47280
4. Mohtai, M., Gupta, M. K., Donlon, B., Ellison, B., Cooke, J., Gibbons, G., Schurman, D. J., and Smith, R. L. (1996) Expression of interleukin-6 in osteoarthritic chondrocytes and effects of fluid-induced shear on this expression in normal human chondrocytes in vitro. J. Orthop. Res. 14, 67-73
5. Zhu, F., Wang, P., Kontrogianni-Konstantopoulos, A., and Konstantopoulos, K. (2010) Prostaglandin (PG)D(2) and 15-deoxy-delta(12,14)-PGJ(2), but not PGE(2), mediate shearinduced chondrocyte apoptosis via protein kinase A-dependent regulation of polo-like kinases. Cell Death Differ. 17, 1325-1334
6. Amin, A. R., Attur, M., Patel, R. N., Thakker, G. D., Marshall, P. J., Rediske, J., Stuchin, S. A., Patel, I. R., and Abramson, S. B. (1997) Superinduction of cyclooxygenase-2 activity in human osteoarthritis-Affected cartilage. Influence of nitric oxide. J. Clin. Invest. 99, 1231-1237
7. Zhu, F., Wang, P., Lee, N. H., Goldring, M. B., and Konstantopoulos, K. (2010) Prolonged application of high fluid shear to chondrocytes recapitulates gene expression profiles associated with osteoarthritis. PLoS One 5, e15174
8. Jacques, C., Sautet, A., Moldovan, M., Thomas, B., Humbert, L., and Berenbaum, F. (1999) Cyclooxygenase activity in chondrocytes from osteoarthritic and healthy cartilage. Rev. Rhum. Engl. Ed. 66, 701-704
9. Brenn, D., Richter, F., and Schaible, H. G. (2007) Sensitization of unmyelinated sensory fibers of the joint nerve to mechanical stimuli by interleukin-6 in the rat: an inflammatory mechanism of joint pain. Arthritis Rheum. 56, 351-359
10. Wang, P., Zhu, F., and Konstantopoulos, K. (2010) Prostaglandin E2 induces interleukin-6 expression in human chondrocytes via cAMP/protein kinase A-And phosphatidylinositol 3-kinase-dependent NF-kappaB activation. Am. J. Physiol. Cell Physiol. 298, C1445-1456
11. Portanova, J. P., Zhang, Y., Anderson, G. D., Hauser, S. D., Masferrer, J. L., Seibert, K., Gregory, S. A., and Isakson, P. C. (1996) Selective neutralization of prostaglandin E2 blocks inflammation, hyperalgesia, and interleukin 6 production in vivo. J. Exp. Med. 184, 883-891
12. Fahmi, H., Di Battista, J. A., Pelletier, J. P., Mineau, F., Ranger, P., and Martel-Pelletier, J. (2001) Peroxisome proliferator-Activated receptor gamma activators inhibit interleukin-1betainduced nitric oxide and matrix metalloproteinase 13 production in human chondrocytes. Arthritis Rheum. 44, 595-607
13. Wang, P., Zhu, F., Tong, Z., and Konstantopoulos, K. (2011) Response of chondrocytes to shear stress: antagonistic effects of the binding partners Toll-like receptor 4 and caveolin-1. FASEB J. 25, 3401-3415
14. Felson, D. T. (2006) Clinical practice. Osteoarthritis of the knee. N. Engl. J. Med. 354, 841-848
15. Towle, C. A., Hung, H. H., Bonassar, L. J., Treadwell, B. V., and Mangham, D. C. (1997) Detection of interleukin-1 in the cartilage of patients with osteoarthritis: a possible autocrine/paracrine role in pathogenesis. Osteoarthritis Cartilage 5, 293-300
16. Afzal, S., and Khanam, A. (2011) Serum estrogen and interleukin-6 levels in postmenopausal female osteoarthritis patients. Pak. J. Pharm. Sci. 24, 217-219
17. Karlsson, C., Dehne, T., Lindahl, A., Brittberg, M., Pruss, A., Sittinger, M., and Ringe, J. (2010) Genome-wide expression profiling reveals new candidate genes associated with osteoarthritis. Osteoarthritis Cartilage 18, 581-592
18. Lems, W. F., and den Uyl, D. (2012) Exercise-induced changes in interleukin-10 in patients with knee osteoarthritis: new perspectives? Arthritis Res. Ther. 12, 131
19. Zhang, R., Fang, H., Chen, Y., Shen, J., Lu, H., Zeng, C., Ren, J., Zeng, H., Li, Z., Chen, S., Cai, D., and Zhao, Q. (2012) Gene expression analyses of subchondral bone in early experimental osteoarthritis by microarray. PLoS One 7, e32356
20. Ohta, S., Imai, K., Yamashita, K., Matsumoto, T., Azumano, I., and Okada, Y. (1998) Expression of matrix metalloproteinase 7 (matrilysin) in human osteoarthritic cartilage. Lab. Invest. 78, 79-87
21. Goldring, M. B. (2000) Osteoarthritis and cartilage: the role of cytokines. Curr. Rheumatol. Rep. 2, 459-465
22. Henderson, B., and Pettipher, E. R. (1989) Arthritogenic actions of recombinant IL-1 and tumour necrosis factor alpha in the rabbit: evidence for synergistic interactions between cytokines in vivo. Clin. Exp. Immunol. 75, 306-310
23. Saklatvala, J. (1986) Tumour necrosis factor alpha stimulates resorption and inhibits synthesis of proteoglycan in cartilage. Nature 322, 547-549
24. Chadjichristos, C., Ghayor, C., Kypriotou, M., Martin, G., Renard, E., Ala-Kokko, L., Suske, G., de Crombrugghe, B., Pujol, J. P., and Galera, P. (2003) Sp1 and Sp3 transcription factors mediate interleukin-1 beta down-regulation of human type II collagen gene expression in articular chondrocytes. J. Biol. Chem. 278, 39762-39772
25. Guerne P. A. Carson D. A. Lotz M. (1990) IL-6production by human articular chondrocytes. Modulation of its synthesis by cytokines, growth factors, and hormones in vitro. J. Immunol. 144, 499-505
26. Lotz, M., Terkeltaub, R., and Villiger, P. M. (1992) Cartilage and joint inflammation. Regulation of IL-8 expression by human articular chondrocytes. J. Immunol. 148, 466-473
27. Villiger, P. M., Terkeltaub, R., and Lotz, M. (1992) Monocyte chemoattractant protein-1 (MCP-1) expression in human articular cartilage. Induction by peptide regulatory factors and differential effects of dexamethasone and retinoic acid. J. Clin. Invest. 90, 488-496
28. Lefebvre, V., Peeters-Joris, C., and Vaes, G. (1990) Modulation by interleukin 1 and tumor necrosis factor alpha of production of collagenase, tissue inhibitor of metalloproteinases and collagen types in differentiated and dedifferentiated articular chondrocytes. Biochim. Biophys. Acta 1052, 366-378
29. Mengshol, J. A., Vincenti, M. P., Coon, C. I., Barchowsky, A., and Brinckerhoff, C. E. (2000) Interleukin-1 induction of collagenase 3 (matrix metalloproteinase 13) gene expression in chondrocytes requires p38, c-Jun N-terminal kinase, and nuclear factor kappaB: differential regulation of collagenase 1 and collagenase 3. Arthritis Rheum. 43, 801-811
30. Reboul, P., Pelletier, J. P., Tardif, G., Cloutier, J. M., and Martel-Pelletier, J. (1996) The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes. A role in osteoarthritis. J. Clin. Invest. 97, 2011-2019
31. Todhunter, P. G., Kincaid, S. A., Todhunter, R. J., Kammermann, J. R., Johnstone, B., Baird, A. N., Hanson, R. R., Wright, J. M., Lin, H. C., and Purohit, R. C. (1996) Immunohistochemical analysis of an equine model of synovitis-induced arthritis. Am. J. Vet. Res. 57, 1080-1093
32. Guccione, A. A., Felson, D. T., Anderson, J. J., Anthony, J. M., Zhang, Y., Wilson, P. W., Kelly-Hayes, M., Wolf, P. A., Kreger, B. E., and Kannel, W. B. (1994) The effects of specific medical conditions on the functional limitations of elders in the Framingham Study. Am. J. Public Health 84, 351-358
33. Orita, S., Koshi, T., Mitsuka, T., Miyagi, M., Inoue, G., Arai, G., Ishikawa, T., Hanaoka, E., Yamashita, K., Yamashita, M., Eguchi, Y., Toyone, T., Takahashi, K., and Ohtori, S. (2011) Associations between proinflammatory cytokines in the synovial fluid and radiographic grading and pain-related scores in 47 consecutive patients with osteoarthritis of the knee. BMC Musculoskelet. Disord. 12, 144
34. Stove, J., Huch, K., Gunther, K. P., and Scharf, H. P. (2000) Interleukin-1beta induces different gene expression of stromelysin, aggrecan and tumor-necrosis-factor-stimulated gene 6 in human osteoarthritic chondrocytes in vitro. Pathobiology 68, 144-149
35. Alaaeddine, N., Di Battista, J. A., Pelletier, J. P., Kiansa, K., Cloutier, J. M., and Martel-Pelletier, J. (1999) Differential effects of IL-8, LIF (pro-inflammatory) and IL-11 (anti-inflammatory) on TNF-Alpha-induced PGE(2)release and on signalling pathways in human OA synovial fibroblasts. Cytokine 11, 1020-1030
36. Yu, C. L., Sun, K. H., Shei, S. C., Tsai, C. Y., Tsai, S. T., Wang, J. C., Liao, T. S., Lin, W. M., Chen, H. L., Yu, H. S., and Han, S. H. (1994) Interleukin 8 modulates interleukin-1 beta, interleukin-6 and tumor necrosis factor-Alpha release from normal human mononuclear cells. Immunopharmacology 27, 207-214
37. Westacott, C. I., and Sharif, M. (1996) Cytokines in osteoarthritis: mediators or markers of joint destruction? Semin. Arthritis Rheum. 25, 254-272
38. Villiger, P. M., Geng, Y., and Lotz, M. (1993) Induction of cytokine expression by leukemia inhibitory factor. J. Clin. Invest. 91, 1575-1581
39. Huang, A., and Campbell, J. (1993) A simple improvement to the Triton lysis procedure for plasmid isolation. BioTechniques 14, 730
40. Ishiguro, N., Ito, T., Ito, H., Iwata, H., Jugessur, H., Ionescu, M., and Poole, A. R. (1999) Relationship of matrix metalloproteinases and their inhibitors to cartilage proteoglycan and collagen turnover: analyses of synovial fluid from patients with osteoarthritis. Arthritis Rheum. 42, 129-136
41. Dahlberg, L., Billinghurst, R. C., Manner, P., Nelson, F., Webb, G., Ionescu, M., Reiner, A., Tanzer, M., Zukor, D., Chen, J., van Wart, H. E., and Poole, A. R. (2000) Selective enhancement of collagenase-mediated cleavage of resident type II collagen in cultured osteoarthritic cartilage and arrest with a synthetic inhibitor that spares collagenase 1 (matrix metalloproteinase 1). Arthritis Rheum. 43, 673-682
42. Baici, A. (1998) Inhibition of extracellular matrix-degrading endopeptidases: problems, comments, and hypotheses. Biol. Chem. 379, 1007-1018
43. Homandberg, G. A. (1999) Potential regulation of cartilage metabolism in osteoarthritis by fibronectin fragments. Front. Biosci. 4, D713-730
44. Jiang, Z., Berceli, S. A., Pfahnl, C. L., Wu, L., Goldman, D., Tao, M., Kagayama, M., Matsukawa, A., and Ozaki, C. K. (2004) Wall shear modulation of cytokines in early vein grafts. J. Vasc. Surg. 40, 345-350
45. Messer, R. L., Mickalonis, J., Lewis, J. B., Omata, Y., Davis, C. M., Brown, Y., and Wataha, J. C. (2008) Interactions between stainless steel, shear stress, and monocytes. J. Biomed. Mater. Res. A 87, 229-235
46. Wang, P., Zhu, F., and Konstantopoulos, K. (2012) The antagonistic actions of endogenous interleukin-1beta and 15-deoxydelta12,14-prostaglandin J2 regulate the temporal synthesis of matrix metalloproteinase-9 in sheared chondrocytes. J. Biol. Chem. 287, 31877-31893
47. Wang, P., Zhu, F., and Konstantopoulos, K. (2011) Interleukin-6 synthesis in human chondrocytes is regulated via the antagonistic actions of prostaglandin (PG)E2 and 15-deoxydelta (12,14)-PGJ2. PLoS One 6, e27630
48. Krizanac-Bengez, L., Mayberg, M. R., Cunningham, E., Hossain, M., Ponnampalam, S., Parkinson, F. E., and Janigro, D. (2006) Loss of shear stress induces leukocyte-mediated cytokine release and blood-brain barrier failure in dynamic in vitro blood-brain barrier model. J. Cell. Physiol. 206, 68-77
49. Carroll, G., McGloughlin, T., O'keeffe, L., Callanan, A., and Walsh, M. (2009) Realistic temporal variations of shear stress modulate MMP-2 and MCP-1 expression in arteriovenous vascular access. Cell. Mol. Bioeng. 2, 591-605
50. Tajima, S., Yokoyama, S., and Yamamoto, A. (1983) Effect of lipid particle size on association of apolipoproteins with lipid. J. Biol. Chem. 258, 10073-10082
51. Naito, K., Takahashi, M., Kushida, K., Suzuki, M., Ohishi, T., Miura, M., Inoue, T., and Nagano, A. (1999) Measurement of matrix metalloproteinases (MMPs) and tissue inhibitor of metalloproteinases-1 (TIMP-1) in patients with knee osteoarthritis: comparison with generalized osteoarthritis. Rheumatology (Oxford) 38, 510-515
52. Wang, P., Zhu, F., Lee, N. H., and Konstantopoulos, K. (2010) Shear-induced interleukin-6 synthesis in chondrocytes: roles of E prostanoid (EP) 2 and EP3 in cAMP/protein kinase A-And PI3-K/Akt-dependent NF-kappaB activation. J. Biol. Chem. 285, 24793-24804
53. Liang, F., Hu, D. Y., Wang, B. Y., Huang, N., Wu, Q., and Chen, H. Q. (2005) [Transcriptional activation of interleukin-8 gene induced by shear stress in human umbilical vein endothelial cells]. Zhonghua Nei Ke Za Zhi 44, 421-424
54. Liang, F., Huang, N., Wang, B., and Chen, H. (2002) [Assessment of the role of TLR-4 in shear-stress-induced IL-8 gene transcription activation in vascular endothelial cells by gene mutation and gene transfection technology]. Sheng. Wu Yi Xue Gong Cheng Xue Za Zhi 19, 667-672
55. Cheng, M., Liu, X., Li, Y., Tang, R., Zhang, W., Wu, J., Li, L., Gang, Y., and Chen, H. (2007) IL-8 gene induction by low shear stress: pharmacological evaluation of the role of signaling molecules. Biorheology 44, 349-360
56. Glossop, J. R., and Cartmell, S. H. (2009) Effect of fluid flow-induced shear stress on human mesenchymal stem cells: differential gene expression of IL1B and MAP3K8 in MAPK signaling. Gene Expr. Patt. 9, 381-388
57. Jiang, J., and Dingledine, R. (2013) Role of prostaglandin receptor EP2 in the regulations of cancer cell proliferation, invasion, and inflammation. J. Pharmacol. Exp. Ther. 344, 360-367
58. Chen, B. C., Liao, C. C., Hsu, M. J., Liao, Y. T., Lin, C. C., Sheu, J. R., and Lin, C. H. (2006) Peptidoglycan-induced IL-6 production in RAW 264.7 macrophages is mediated by cyclooxygenase-2, PGE2/PGE4 receptors, protein kinase A, I kappa B kinase, and NF-kappa B. J. Immunol. 177, 681-693
59. Li, L., Tatake, R. J., Natarajan, K., Taba, Y., Garin, G., Tai, C., Leung, E., Surapisitchat, J., Yoshizumi, M., Yan, C., Abe, J., and Berk, B. C. (2008) Fluid shear stress inhibits TNF-mediated JNK activation via MEK5-BMK1 in endothelial cells. Biochem. Biophys. Res. Commun. 370, 159-163
60. Wang, H., Young, S. R., Gerard-O'Riley, R., Hum, J. M., Yang, Z., Bidwell, J. P., and Pavalko, F. M. (2011) Blockade of TNFR1signaling: A role of oscillatory fluid shear stress in osteoblasts. J. Cell. Physiol. 226, 1044-1051
61. Roman-Blas, J. A., and Jimenez, S. A. (2006) NF-kappaB as a potential therapeutic target in osteoarthritis and rheumatoid arthritis. Osteoarthritis Cartilage 14, 839-848
62. Murphy, G., and Nagase, H. (2008) Reappraising metalloproteinases in rheumatoid arthritis and osteoarthritis: destruction or repair? Nat. Clin. Pract. Rheumatol. 4, 128-135
63. Sweeney, V., Cummins, P. M., Birney, Y. A., Cullen, J. P., Redmond, E. M., and Cahill, P. A. (2004) Cyclic strainmediated regulation of endothelial matrix metalloproteinase-2 expression and activity. Cardiovasc. Res. 63, 625-634
64. Zheng, L., Huang, Y., Song, W., Gong, X., Liu, M., Jia, X., Zhou, G., Chen, L., Li, A., and Fan, Y. (2012) Fluid shear stress regulates metalloproteinase-1 and 2 in human periodontal ligament cells: involvement of extracellular signal-regulated kinase (ERK) and P38 signaling pathways. J. Biomech. 45, 2368-2375
65. Kusano, K., Miyaura, C., Inada, M., Tamura, T., Ito, A., Nagase, H., Kamoi, K., and Suda, T. (1998) Regulation of matrix metalloproteinases (MMP-2,-3,-9, and-13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology 139, 1338-1345
66. Liang, K. C., Lee, C. W., Lin, W. N., Lin, C. C., Wu, C. B., Luo, S. F., and Yang, C. M. (2007) Interleukin-1beta induces MMP-9 expression via p42/p44 MAPK, p38 MAPK, JNK, and nuclear factor-kappaB signaling pathways in human tracheal smooth muscle cells. J. Cell. Physiol. 211, 759-770
67. Okada, M., Yamawaki, H., and Hara, Y. Angiotensin II enhances interleukin-1 beta-induced MMP-9 secretion in adult rat cardiac fibroblasts. J. Vet. Med. Sci. 72, 735-739
68. Fleenor, D. L., Pang, I. H., and Clark, A. F. (2003) Involvement of AP-1 in interleukin-1alpha-stimulated MMP-3 expression in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 44, 3494-3501
69. Choi, Y. A., Lee, D. J., Lim, H. K., Jeong, J. H., Sonn, J. K., Kang, S. S., and Baek, S. H. (2004) Interleukin-1beta stimulates matrix metalloproteinase-2 expression via a prostaglandin E2-dependent mechanism in human chondrocytes. Exp. Mol. Med. 36, 226-232
70. Ma, B., van Blitterswijk, C. A., and Karperien, M. (2012) A Wnt/beta-catenin negative feedback loop inhibits interleukin-1-induced matrix metalloproteinase expression in human articular chondrocytes. Arthritis Rheum. 64, 2589-2600
71. Miller, C., Zhang, M., He, Y., Zhao, J., Pelletier, J. P., Martel-Pelletier, J., and Di Battista, J. A. (1998) Transcriptional induction of cyclooxygenase-2 gene by okadaic acid inhibition of phosphatase activity in human chondrocytes: co-stimulation of AP-1 and CRE nuclear binding proteins. J. Cell. Biochem. 69, 392-413
72. Saunders, M. A., Sansores-Garcia, L., Gilroy, D. W., and Wu, K. K. (2001) Selective suppression of CCAAT/enhancer-binding protein beta binding and cyclooxygenase-2 promoter activity by sodium salicylate in quiescent human fibroblasts. J. Biol. Chem. 276, 18897-18904
73. Thomas, B., Berenbaum, F., Humbert, L., Bian, H., Bereziat, G., Crofford, L., and Olivier, J. L. (2000) Critical role of C/EBPdelta and C/EBPbeta factors in the stimulation of the cyclooxygenase-2 gene transcription by interleukin-1beta in articular chondrocytes. Eur. J. Biochem. 267, 6798-6809
74. Abulencia, J. P., Gaspard, R., Healy, Z. R., Gaarde, W. A., Quackenbush, J., and Konstantopoulos, K. (2003) Shear-induced cyclooxygenase-2 via a JNK2/c-Jun-dependent pathway regulates prostaglandin receptor expression in chondrocytic cells. J. Biol. Chem. 278, 28388-28394
75. Alshihabi, S. N., Chang, Y. S., Frangos, J. A., and Tarbell, J. M. (1996) Shear stress-induced release of PGE2 and PGI2 by vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 224, 808-814
76. Gilroy, D. W., Colville-Nash, P. R., Willis, D., Chivers, J., Paul-Clark, M. J., and Willoughby, D. A. (1999) Inducible cyclooxygenase may have anti-inflammatory properties. Nat. Med. 5, 698-701
77. Schuligoi, R., Grill, M., Heinemann, A., Peskar, B. A., and Amann, R. (2005) Sequential induction of prostaglandin E and D synthases in inflammation. Biochem. Biophys. Res. Commun. 335, 684-689
78. Rola-Pleszczynski, M., and Stankova, J. (1992) Cytokine gene regulation by PGE(2), LTB(4) and PAF. Mediators Inflamm. 1, 5-8
79. Sottile, A., Venza, I., Venza, M., Valenti, A., and Teti, D. (1996) PGE2-induced immunoregulation mediated by cytokine production from cultures of human peripheral T lymphocytes. Immunopharmacol. Immunotoxicol. 18, 27-36
80. Harizi, H., and Gualde, N. (2006) Pivotal role of PGE2 and IL-10 in the cross-regulation of dendritic cell-derived inflammatory mediators. Cell. Mol. Immunol. 3, 271-277
81. Alfranca, A., Lopez-Oliva, J. M., Genis, L., Lopez-Maderuelo, D., Mirones, I., Salvado, D., Quesada, A. J., Arroyo, A. G., and Redondo, J. M. (2008) PGE2 induces angiogenesis via MT1-MMP-mediated activation of the TGFbeta/Alk5 signaling pathway. Blood 112, 1120-1128
82. Nishitani, K., Ito, H., Hiramitsu, T., Tsutsumi, R., Tanida, S., Kitaori, T., Yoshitomi, H., Kobayashi, M., and Nakamura, T. (2010) PGE2 inhibits MMP expression by suppressing MKK4-JNK MAP kinase-c-JUN pathway via EP4 in human articular chondrocytes. J. Cell. Biochem. 109, 425-433
83. Martel-Pelletier, J., Pelletier, J. P., and Fahmi, H. (2003) Cyclooxygenase-2 and prostaglandins in articular tissues. Semin. Arthritis Rheum. 33, 155-167
84. Lowe, G. N., Fu, Y. H., McDougall, S., Polendo, R., Williams, A., Benya, P. D., and Hahn, T. J. (1996) Effects of prostaglandins on deoxyribonucleic acid and aggrecan synthesis in the RCJ 3.1C5.18 chondrocyte cell line: role of second messengers. Endocrinology 137, 2208-2216
85. Zayed, N., Afif, H., Chabane, N., Mfuna-Endam, L., Benderdour, M., Martel-Pelletier, J., Pelletier, J. P., Motiani, R. K., Trebak, M., Duval, N., and Fahmi, H. (2008) Inhibition of interleukin-1beta-induced matrix metalloproteinases 1 and 13 production in human osteoarthritic chondrocytes by prostaglandin D2. Arthritis Rheum. 58, 3530-3540
86. Alves, C., de Melo, N., Fraceto, L., de Araujo, D., and Napimoga, M. (2011) Effects of 15d-PGJ(2)-loaded poly(D,L-lactide-co-glycolide) nanocapsules on inflammation. Br. J. Pharmacol. 162, 623-632
87. Storer, P. D., Xu, J., Chavis, J. A., and Drew, P. D. (2005) Cyclopentenone prostaglandins PGA2 and 15-deoxy-delta12,14 PGJ2 suppress activation of murine microglia and astrocytes: implications for multiple sclerosis. J. Neurosci. Res. 80, 66-74
88. Alleva, D. G., Johnson, E. B., Lio, F. M., Boehme, S. A., Conlon, P. J., and Crowe, P. D. (2002) Regulation of murine macrophage proinflammatory and anti-inflammatory cytokines by ligands for peroxisome proliferator-Activated receptor-gamma: counter-regulatory activity by IFN-gamma. J. Leukoc. Biol. 71, 677-685
89. Martinez, A. E., Sanchez-Gomez, F. J., Diez-Dacal, B., Oeste, C. L., and Perez-Sala, D. (2012) 15-Deoxy-Delta(12,14)-prostaglandin J2 exerts pro-And anti-inflammatory effects in mesangial cells in a concentration-dependent manner. Inflamm. Allergy Drug Targets 11, 58-65
90. Chiba, T., Ueki, S., Ito, W., Kato, H., Takeda, M., Kayaba, H., Furue, M., and Chihara, J. (2009) 15-Deoxy-Delta(12,14)-prostaglandin J2 induces IL-8 and GM-CSF in a human airway epithelial cell line (NCI-H292). Int. Arch. Allergy Immunol. 149(Suppl. 1), 77-82
91. Fahmi, H., Pelletier, J. P., Di Battista, J. A., Cheung, H. S., Fernandes, J. C., and Martel-Pelletier, J. (2002) Peroxisome proliferator-Activated receptor gamma activators inhibit MMP-1 production in human synovial fibroblasts likely by reducing the binding of the activator protein 1. Osteoarthritis Cartilage 10, 100-108
92. Pustovrh, M. C., Capobianco, E., Martinez, N., Higa, R., White, V., and Jawerbaum, A. (2009) MMP/TIMP balance is modulated in vitro by 15dPGJ(2) in fetuses and placentas from diabetic rats. Eur. J. Clin. Invest. 39, 1082-1090
93. Piva, R., Gianferretti, P., Ciucci, A., Taulli, R., Belardo, G., and Santoro, M. G. (2005) 15-Deoxy-delta 12,14-prostaglandin J2 induces apoptosis in human malignant B cells: an effect associated with inhibition of NF-kappa B activity and downregulation of antiapoptotic proteins. Blood 105, 1750-1758
94. Liu, J. J., Huang, R. W., Lin, D. J., Peng, J., Wu, X. Y., Lin, Q., Pan, X. L., Song, Y. Q., Zhang, M. H., Hou, M., and Chen, F. (2005) Expression of survivin and bax/bcl-2 in peroxisome proliferator activated receptor-gamma ligands induces apoptosis on human myeloid leukemia cells in vitro. Ann. Oncol. 16, 455-459
95. Cippitelli, M., Fionda, C., Di Bona, D., Lupo, A., Piccoli, M., Frati, L., and Santoni, A. (2003) The cyclopentenone-type prostaglandin 15-deoxy-delta12,14-prostaglandin J2 inhibits CD95 ligand gene expression in t lymphocytes: interference with promoter activation via peroxisome proliferator-Activated receptor-gamma-independent mechanisms. J. Immunol. 170, 4578-4592
96. Nishida, K., Kunisada, T., Shen, Z. N., Kadota, Y., Hashizume, K., and Ozaki, T. (2008) Chondrosarcoma and peroxisome proliferator-Activated receptor. PPAR Res. 2008, 250568
97. Shan, Z. Z., Masuko-Hongo, K., Dai, S. M., Nakamura, H., Kato, T., and Nishioka, K. (2004) A potential role of 15-deoxydelta (12,14)-prostaglandin J2 for induction of human articular chondrocyte apoptosis in arthritis. J. Biol. Chem. 279, 37939-37950
98. Laine, L., White, W. B., Rostom, A., and Hochberg, M. (2008) COX-2 selective inhibitors in the treatment of osteoarthritis. Semin. Arthritis Rheum. 38, 165-187
99. Kobayashi, M., Squires, G. R., Mousa, A., Tanzer, M., Zukor, D. J., Antoniou, J., Feige, U., and Poole, A. R. (2005) Role of interleukin-1 and tumor necrosis factor alpha in matrix degradation of human osteoarthritic cartilage. Arthritis Rheum. 52, 128-135
100. Boileau, C., Pelletier, J. P., Tardif, G., Fahmi, H., Laufer, S., Lavigne, M., and Martel-Pelletier, J. (2005) The regulation of human MMP-13 by licofelone, an inhibitor of cyclo-oxygenases and 5-lipoxygenase, in human osteoarthritic chondrocytes is mediated by the inhibition of the p38 MAP kinase signalling pathway. Ann. Rheum. Dis. 64, 891-898 Skin Diseases